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Toward a unified connectomic target for deep brain stimulation in obsessive-compulsive disorder

View ORCID ProfileNingfei Li, Juan Carlos Baldermann, Astrid Kibleur, Svenja Treu, Harith Akram, Gavin J.B. Elias, Alexandre Boutet, Andres M. Lozano, Bassam Al-Fatly, Bryan Strange, Juan Barcia, Ludvic Zrinzo, Eileen Joyce, Stephan Chabardes, Veerle Visser-Vandewalle, Mircea Polosan, Jens Kuhn, Andrea A. Kühn, Andreas Horn
doi: https://doi.org/10.1101/608786
Ningfei Li
1Movement Disorders & Neuromodulation Unit, Department for Neurology, Charité University Medicine Berlin, Germany
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  • ORCID record for Ningfei Li
  • For correspondence: ningfei.li@charite.de
Juan Carlos Baldermann
2Department of Psychiatry and Psychotherapy, University of Cologne, Medical faculty, Cologne, Germany
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Astrid Kibleur
3Univ. Grenoble Alpes, F-38000 Grenoble, France
4OpenMind Innovation, F-75008 Paris, France
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Svenja Treu
5Laboratory for Clinical Neuroscience, Centre for Biomedical Technology, Universidad Politecnica de Madrid, Spain
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Harith Akram
7Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, London, UK
8National Hospital for Neurology and Neurosurgery, UCL Queen Square Institute of Neurology, London, UK
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Gavin J.B. Elias
9University Health Network, Toronto, Ontario, Canada
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Alexandre Boutet
9University Health Network, Toronto, Ontario, Canada
10Joint Department of Medical Imaging, University of Toronto, Ontario, Canada
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Andres M. Lozano
9University Health Network, Toronto, Ontario, Canada
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Bassam Al-Fatly
1Movement Disorders & Neuromodulation Unit, Department for Neurology, Charité University Medicine Berlin, Germany
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Bryan Strange
5Laboratory for Clinical Neuroscience, Centre for Biomedical Technology, Universidad Politecnica de Madrid, Spain
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Juan Barcia
6Hospital Clínico San Carlos, Neurosurgery Department, Universidad Complutense de Madrid, Spain
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Ludvic Zrinzo
7Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, London, UK
8National Hospital for Neurology and Neurosurgery, UCL Queen Square Institute of Neurology, London, UK
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Eileen Joyce
7Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, London, UK
8National Hospital for Neurology and Neurosurgery, UCL Queen Square Institute of Neurology, London, UK
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Stephan Chabardes
3Univ. Grenoble Alpes, F-38000 Grenoble, France
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Veerle Visser-Vandewalle
11Department of Stereotactic and Functional Neurosurgery, University of Cologne, Cologne, Germany
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Mircea Polosan
3Univ. Grenoble Alpes, F-38000 Grenoble, France
12Inserm, U1216, Grenoble Institut des Neurosciences, F-38000 Grenoble, France
13Psychiatry Department, CHU Grenoble Alpes, F-38000 Grenoble, France
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Jens Kuhn
2Department of Psychiatry and Psychotherapy, University of Cologne, Medical faculty, Cologne, Germany
14Johanniter Hospital Oberhausen, EVKLN, Department of Psychiatry, Psychotherapy and Psychosomatics, Oberhausen, Germany
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Andrea A. Kühn
1Movement Disorders & Neuromodulation Unit, Department for Neurology, Charité University Medicine Berlin, Germany
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Andreas Horn
1Movement Disorders & Neuromodulation Unit, Department for Neurology, Charité University Medicine Berlin, Germany
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Abstract

Multiple surgical targets have been proposed for treating obsessive-compulsive disorder (OCD) with deep brain stimulation (DBS). However, different targets may modulate the same neural network responsible for clinical improvement. Here we analyzed data from four cohorts of OCD patients (N = 50) that underwent DBS to the anterior limb of the internal capsule (ALIC), the nucleus accumbens (NAcc) or the subthalamic nucleus (STN). Fiber tracts that were predominantly connected to electrodes in good or poor DBS responders were isolated from a normative structural connectome and assigned a predictive value. Strikingly, the same fiber bundle was related to treatment response when independently analyzing two large training cohorts that targeted either ALIC or STN. This discriminative tract is a subsection of the ALIC and connects frontal regions (such as the dorsal anterior cingulate, dACC, and ventral prefrontal, vlPFC, cortices to the STN). When informing the tract solely based on one cohort (e.g. ALIC), clinical improvements in the other (e.g. STN) could be significantly predicted, and vice versa. Finally, clinical improvements of eight patients from a third center with electrodes in the NAcc and six patients from a fourth center in which electrodes had been implanted in both STN and ALIC were significantly predicted based on this novel tract-based DBS target. Results suggest a functional role of a limbic hyperdirect pathway that projects from dACC and vlPFC to anteriomedial STN. Obsessive-compulsive symptoms seem to be tractable by modulating the specific bundle isolated here. Our results show that connectivity-derived improvement models can inform clinical improvement across DBS targets, surgeons and centers. The identified tract is now three-dimensionally defined in stereotactic standard space and will be made openly available.

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Posted March 19, 2020.
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Toward a unified connectomic target for deep brain stimulation in obsessive-compulsive disorder
Ningfei Li, Juan Carlos Baldermann, Astrid Kibleur, Svenja Treu, Harith Akram, Gavin J.B. Elias, Alexandre Boutet, Andres M. Lozano, Bassam Al-Fatly, Bryan Strange, Juan Barcia, Ludvic Zrinzo, Eileen Joyce, Stephan Chabardes, Veerle Visser-Vandewalle, Mircea Polosan, Jens Kuhn, Andrea A. Kühn, Andreas Horn
bioRxiv 608786; doi: https://doi.org/10.1101/608786
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Toward a unified connectomic target for deep brain stimulation in obsessive-compulsive disorder
Ningfei Li, Juan Carlos Baldermann, Astrid Kibleur, Svenja Treu, Harith Akram, Gavin J.B. Elias, Alexandre Boutet, Andres M. Lozano, Bassam Al-Fatly, Bryan Strange, Juan Barcia, Ludvic Zrinzo, Eileen Joyce, Stephan Chabardes, Veerle Visser-Vandewalle, Mircea Polosan, Jens Kuhn, Andrea A. Kühn, Andreas Horn
bioRxiv 608786; doi: https://doi.org/10.1101/608786

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